The resonant component of human physiological hand tremor is altered by slow voluntary movements

Abstract

Key points• Postural physiological hand tremor has a prominent component at ∼8 Hz unlike the associated EMG. Consequently, the gain between EMG and tremor is sharply peaked at ∼8 Hz.• Deduction and a simple model using pre-recorded EMG or random noise as an input show that the ∼8 Hz peak is a consequence of resonance.• During voluntary movement the gain peak enlarges and shifts to a lower frequency but the EMG spectrum shows no corresponding changes. This reflects muscle thixotropy. Adjustment of the muscle properties of the model reproduces the effect.• These findings suggest that the rhythm of hand tremor in posture and movement is related to muscle and limb mechanics rather than a neural oscillator.• The discovery that the gain relating EMG to acceleration is very different when static and moving has implications for the control of movement in health and disease.Abstract Limb resonance imparts a characteristic spectrum to hand tremor. Movement will alter the resonance. We have examined the consequences of this change. Rectified forearm extensor muscle EMG and physiological hand tremor were recorded. In postural conditions the EMG spectrum is relatively flat whereas the acceleration spectrum is sharply peaked. Consequently, the gain between EMG and acceleration is maximal at the frequency where the tremor is largest (∼8 Hz). The shape of the gain curve implies mechanical resonance. Substantial alterations in posture do not significantly change the characteristics of the tremor or the shape or size of the gain curve. By contrast, slow or moderately paced voluntary wrist flexion-extension movements dramatically increase the hand tremor size and lower its peak frequency. These changes in size and frequency of the tremor cannot be attributed to changes in the EMG. Instead they reflect a very large change in the size and shape of the gain curve relating EMG to acceleration. The gain becomes larger and the peak moves to a lower frequency (∼6 Hz). We suggest that a movement-related (thixotropic) alteration in resonant properties of the wrist provides a simple explanation for these changes. The mechanism is illustrated by a model. Our new findings confirm that resonance plays a major role in wrist tremor. We also demonstrate that muscles operate very differently under postural and dynamic conditions. The different coupling between EMG and movement in posture and when moving must pose a considerable challenge for neural predictive control of skeletal muscles.

The Selective Influence of Rhythmic Cortical versus Cerebellar Transcranial Stimulation on Human Physiological Tremor

“…Our data also tend to refute the hypothesis that physiological tremor, whether postural or kinetic, is exclusively mediated by peripheral and/or spinal mechanisms (Joyce and Rack, 1974;Lakie et al, 1986Lakie et al, , 2012Vernooij et al, 2013). This hypothesis posits that physiological tremor is either the consequence of broad-band forcing of a nonlinear, resonant system, and that synchronous central input is not required (Vernooij et al, 2013), or that it reflects frequency components in the band of the firing rates of last-recruited, large motor units (Christakos et al, 2006), or that local oscillatory reflex loops induce synchronous motor unit activity at the level of the spinal cord (Lippold, 1970;Christakos et al, 2006).…”

“…Several lines of evidence suggest that physiological tremor is secondary to central oscillatory activity (Conway et al, 1995;Vallbo, 1995a, b, 1996;Elble, 1996;Kakuda et al, 1999;Wessberg and Kakuda, 1999;Duval et al, 2000Duval et al, , 2005McAuley and Marsden, 2000;Gross et al, 2002;Evans and Baker, 2003;Jaberzadeh et al, 2003;Proudlock and Scott, 2003;Bye and Neilson, 2010). However, mechanical resonance of the limb alone has been shown to be sufficient to produce a characteristic physiological tremor spectrum (Vernooij et al, 2013), and it has been argued that the apparent motor unit synchronization and observations of corticomuscular coherence with tremor are epiphenomenal and a mere consequence of peripheral resonance (Lakie et al, 2012).…”

A dominant role for mechanical resonance in physiological finger tremor revealed by selective minimization of voluntary drive and movement

“…This corresponded to the peak frequency of isotonic hand acceleration, leading the authors to conclude that the primary cause of tremor was the stretch reflex. However, a number of other studies have shown that the peak frequency of hand tremor does not match the peak frequency of the demodulated EMG (for example, Raethjen et al 2000;Timmer et al 1998), and this has been confirmed by recent studies on hand tremor from our laboratory (Lakie et al 2012;Reynolds and Lakie 2010). In the present study, we systematically examine physiological finger tremor when the finger is fixed or free to move.…”

“…This has lead to a "bump" model which seeks to explain physiological tremor in terms of rhythmic central drive (Bye and Neilson 2010). However, in recent work on hand tremor we have observed that all of the characteristics of tremor and pulsation during movement can be satisfactorily reproduced by a resonator driven by a noisy EMG input (Lakie et al 2012). The evidence for relevant central oscillators is tenuous, and here we test the idea that the distinguishing features of physiological tremor do not require any central drive.…”

“…In particular, we examine the gain between EMG and acceleration or force to determine how the musculoskeletal system acts at different frequencies. Since our recently published study (Lakie et al 2012) suggests that tremor frequency and amplitude are altered by movement, we also incorporate different levels of muscular activation and movement.…”